Climate change, phenology, and butterfly host plant utilization

Climate change, phenology, and butterfly host plant utilization

Jose A. Navarro-Cano, Bengt Karlsson, Diana Posledovich, Tenna Toftegaard,

Christer Wiklund, Johan Ehrlen, Karl Gotthard

Abstract Knowledge of how species interactions are

influenced by climate warming is paramount to understand

current biodiversity changes. We review phenological

changes of Swedish butterflies during the latest decades

and explore potential climate effects on butterfly–host plant

interactions using the Orange tip butterfly Anthocharis

cardamines and its host plants as a model system. This

butterfly has advanced its appearance dates substantially,

and its mean flight date shows a positive correlation with

latitude. We show that there is a large latitudinal variation

in host use and that butterfly populations select plant

individuals based on their flowering phenology. We

conclude that A. cardamines is a phenological specialist but

a host species generalist. This implies that thermal

plasticity for spring development influences host utilization

of the butterfly through effects on the phenological

matching with its host plants. However, the host utilization

strategy of A. cardamines appears to render it resilient to

relatively large variation in climate.

Keywords Brassicaceae � Diet width � Herbivory �Latitude � Lepidoptera � Species interactions

INTRODUCTION

Climate change is considered one of the biggest threats to

biodiversity today, and many species risk extinction due to a

changed climate (Thomas et al. 2004; Parmesan 2006; Cahill

et al. 2013). Species interactions make up an important part

of biodiversity. Yet, knowledge of how such interactions are

influenced by climate and habitat change is comparatively

sparse (Lavergne et al. 2010). A change in climate or other

environmental conditions may influence the strength of

species interactions by relatively rapid plastic responses and

by evolutionary changes over generations (Visser and Both

2005; Visser 2008; Altermatt 2010; Singer and Parmesan

2010). For example, if the phenology of an herbivore and its

host plants in a seasonal environment is differentially influ-

enced by temperature, a change in climate may lead to

changes in the temporal overlap between the herbivore and

its hosts (e.g., Singer and Parmesan 2010). As a result, the

intensity of the interaction might change, or it may even

disappear (Dewar and Watt 1992; Harrington et al. 1999). In

herbivores using multiple hosts, climate change may lead to

changes in the relative overlap with different hosts and thus

to changes in host use. Such changes in interaction patterns

are important to study as they influence both population

dynamics and selection regimes, and are fundamental to

understand how climate change might influence natural

communities (Visser 2008).

A clear trend among many temperate species, including

birds, plants and insects, during the past decades is that

they have started to reproduce earlier during the spring and

summer (Walther et al. 2002; Menzel et al. 2006; Parmesan

2007). Butterflies are temperature sensitive and all their life

history stages are influenced by temperature (e.g., Dennis

1993; Karlsson and Wiklund 2005). Several studies have

observed positive correlations between ambient tempera-

tures during growth and development and date of the adult

flight period, with an average advancement around 4 days/

�C (Sparks and Yates 1997; Karlsson 2013). Some authors

have also documented recent advancements in butterfly

phenology in response to a warmer climate (Sparks and

Yates 1997; Stefanescu et al. 2003; Menzel et al. 2006;

Altermatt 2010; Diamond et al. 2011; Karlsson 2013).

Electronic supplementary material The online version of thisarticle (doi:10.1007/s13280-014-0602-z) contains supplementarymaterial, which is available to authorized users.

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AMBIO 2015, 44(Suppl. 1):S78–S88

DOI 10.1007/s13280-014-0602-z

However, recent comparative studies of butterflies in the

UK (Diamond et al. 2011) and in Sweden (Karlsson 2013)

reveal that shifts in phenology show a profound variation

among species, making a more thorough inspection of the

phenological responses justified. Previous studies have

shown that variation in phenology shifts among butterfly

species is associated with several life history traits,

including overwintering stage, seasonal appearance, food

plant species as well as several other factors, like food

availability, habitat, altitude, and latitude (Altermatt 2010,

2012; Diamond et al. 2011; Illan et al. 2012; Karlsson

2013). For example, species overwintering as adults or as

pupae tend to advance their phenology more than species

overwintering as larvae or in their egg stage (Altermatt

2010; Diamond et al. 2011; Karlsson 2013).

Butterflies critically depend on plants as larval hosts and

for nectar, and it is likely that optimal butterfly phenology in

many cases strongly depends on the phenology of their host

plants. Butterflies and host plants may respond differently to

a warming climate, either because they use partly different

cues or because their sensitivity to given cues differ (e.g.,

Menzel and Fabian 1999; Menzel et al. 2001; Parmesan

2007). Moreover, the direct effects of increased availability

of CO2 may affect plant phenology more than the insects that

use them as a resource. The relative importance of cues also

varies among plants species (e.g., Rathcke and Lacey 1985),

which may result in climate-dependent variation in relative

abundances of different host species during the period of

reproduction and growth of the butterflies (Schweiger et al.

2008). Such differences in reaction norms should lead to

changes in species interactions with changes in climate.

Given that butterflies are strongly selected to maximize

synchrony with their host plants and that host plants to

some extent differ from each other and from butterflies in

their response to increased temperatures, we expect but-

terfly responses to be related to the specific set of host

plants that they depend on. For example, Diamond et al.

(2011) showed that butterfly species with a small diet

breadth, i.e., with only a few species of larval host plants,

have higher advancement rates compared to species with a

large repertoire of host plants. It can also be expected that

butterfly species that feed exclusively on specific devel-

opmental stages of their hosts, e.g., flowers, young fruits, or

young leaves, shift their phenology more strongly in

response to warming than species that are not restricted to

specific developmental stages.

An additional factor affecting plant and animal phe-

nology is geographic location. The effects of latitude have

been extensively scrutinized, and due to climate gradients

stretching from south to north, growth and reproduction are

generally occurring later in the northern parts (e.g., Myneni

et al. 1997; Karlsen et al. 2007; Rotzer and Chmielewski

2001; Doi and Takahashi 2008). Butterflies show a

relatively straightforward pattern with northern populations

flying at later dates (Roy and Asher 2003; Karlsson 2013).

However, not only phenology may vary along latitudinal

gradients, but also the relative importance of different cues.

Such differences would imply that plant populations of the

same species along a latitudinal gradient respond differ-

ently to climate warming. This may lead to different

responses among butterfly populations in order to maxi-

mize synchronization. Moreover, many butterfly species

depend on multiple host plants, which use partly different

environmental cues for start of development and that vary

in relative abundance along latitudinal gradients. In com-

bination, these relationships suggest that the realized pat-

tern of host use will be affected by variation in climate,

whether it is due to latitudinal differences or to long-term

climate change. Such climate effects on host use are likely

to be particularly important in butterfly species that are

specializing on feeding on a specific phenological stage of

their hosts. However, the effects of climate variation on

patterns of host utilization in phenological specialists have

rarely been studied. Indeed, detailed data on climate-

induced changes of insect–host plant interactions over long

periods of time are overall very rare (Visser and Both 2005;

Singer and Parmesan 2010). One way forward is therefore

to explore spatial variation in butterfly–host interactions

along the climatic gradients of latitude or altitude.

Here, we review phenological changes in temperate

butterflies over the last decades in Sweden and present

results from an ongoing project exploring variation in the

interaction between one phenological specialist, Antho-

charis cardamines, and its multiple host plants along a

latitudinal cline representing large variation in climate.

More specifically we ask (1) How much has mean flight

date changed in butterfly species in general, and in A.

cardamines in particular, during the last 20 years in the

same geographical area? (2) How well do temporal chan-

ges in mean flight dates for these species agree with the

spatial trend along a latitudinal gradient? (3) To what

degree do life history traits such as voltinism and over-

wintering stage correlate with changes in mean flight dates

of butterflies in general? and (4) How does among- and

within-species host plant use in Anthocharis cardamines

differs along a latitudinal gradient?

MATERIALS AND METHODS

Study system

The focal butterfly species in this study, the Orange-tip

Anthocharis cardamines (Lepidoptera: Pieridae), and its

host plant species constitute a particularly interesting

model system to assess potential climate-dependent effects

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on host use. This butterfly is oligophagous on Brassicaceae

using up to 17 different Brassicaceae species from 14

different genera within their range in Sweden (Wiklund

and Ahrberg 1978; Arvanitis et al. 2007). The species is a

phenological specialist in the sense that it feeds only on

flowers and seedpods of its host, which are available for a

period of approximately 1 month in spring at any given

location in Sweden (Wiklund and Ahrberg 1978; Wiklund

and Friberg 2009). As a result of its dependence of host

plants that flower relatively early, A. cardamines flies early

in the season (Fig. 1). Although both the butterfly and its

host plants have a wide distribution in Europe, A. card-

amines is obligatory univoltine and after larval develop-

ment in spring, it pupates and enters diapause in early

summer. Thus, the species spends most of the summer, and

all of autumn and winter in the pupal stage.

Changes in mean flight dates across butterfly species

We used the dataset compiled by Karlsson (2013) from the

public database Swedish Species Gateway (http://www.

artportalen.se) that contains observations of both amateur

and professional naturalists. Using these data, we explore

correlations between life history traits (voltinism, diapause

stage) and temporal and latitudinal trends in phenology

(mean flight date) of 66 butterfly species in Sweden and

relate it to the special case of A. cardamines. For more

detailed information about the data compilation, see Kar-

lsson (2013).

Study design latitudinal variation in A. cardamines

host plant use

For our study of latitudinal variation in host plant use of

Anthocharis cardamines, we included six host plant spe-

cies: two perennial herbs: Cardamine pratensis L. and

Arabis hirsuta (L.) Scop., one biennial: A. glabra (L.)

Bernh., and three annuals: Arabidopsis thaliana (L.) Hey-

nh., Capsella bursa-pastoris (L.) Medik., and Thlaspi

caerulescens (J. Presl and C. Presl). C. pratensis grows on

meadows, marshes, ditches, and stream margins (Arvanitis

et al. 2007), whereas the other species use different habitats

such as meadows, hillocks, rocks, and roadsides (Wiklund

and Friberg 2009). Arabidopsis thaliana and T. caerules-

cens are the earliest species, flowering from March to

April, and A. glabra and C. pratensis are the latest ones

(June–July). Capsella bursa-pastoris has an extended

flowering period (April to October) (Mossberg and Sten-

berg 2010). We distinguished between the tetraploid

C. pratensis ssp. pratensis (hereafter, C. pratensis) and the

octoploid C. pratensis ssp. paludosa (Knaf) Kvet. (here-

after, C. paludosa), based on flower size and the type of

cauline leaves (Arvanitis et al. 2007). These seven plant

taxa span along the Swedish coast but their abundance

varies from South to North (Mossberg and Stenberg 2010).

A latitudinal delay in flowering from South to North within

each species is expected as a consequence of the average

monthly temperature, which is roughly correlated with the

plant growing season (Sjors 1999).

Fig. 1 Anthocharis cardamines flying period and observation frequency (number of regional observations) in south (black line), central (dark

gray line), and north (gray line) regions according to the 2010 ‘‘species gateway’’ data base (http://www.artportalen.se). Data were fitted to a

Gaussian curve. Vertical dashed lines indicate the starting date of our samplings. Distribution map: Eliasson et al. (2005); Photograph by Christer

Wiklund shows a male A. cardamines nectaring on Cardamine pratensis

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Data were collected between 17 May and 16 June 2010.

We selected three regions ranging a 900 km S–N climatic

gradient along the Eastern Swedish coast (Electronic

Supplementary Material, Fig. S1): regions South (Scania

Province; 55�490N, 14�050E), Centre (Uppland; 59�300N,

18�350E), and North (Angermanland; 63�030N, 18�190E).

We sampled consecutively in S (17–23 May), in C (28

May–3 June), and N (10–16 June). Within each region,

1–11 populations per host plant species were sampled in an

area of approximately 50 km2 (Table 1).

We sampled data both at the level of plots and at the level of

plant individuals. In each region, we searched randomly for

occurrences of host plants. Whenever patches of one or mul-

tiple host plants were found, we established study plots. A plot

was defined as the area covered by a patch of single or mixed

host species populations, which was separated from the closest

patch by at least 25 m. We judge that this design resulted in that

differences in abundances among species in surveyed plots,

roughly reflected abundances within the larger study region. At

the plot level, we estimated the plot area including all the host

plants in a patch as well as the total number of host plant

individuals per species, yielding estimates of densities for each

of the host plant species. Plot area ranged from 18 to 5382 m2.

We searched all plants within plots for presence of butterfly

eggs and estimated the mean number of eggs per plant within

each plot as the total number of eggs divided by the number of

plants individuals. At the individual level, we measured traits

for a random subsample of the plants scored for each popu-

lation. In populations with less than 100 plants, all plants were

measured, whereas random samples of up to 150 plants were

measured in larger populations. The measured traits were

plant size (maximum shoot length), the total number of

flowers on all shoots (total number of buds ? flowers ? pods

at the time of recording), and the phenological state (number

of pods divided by the total number of flowers at the time of

recording). Overall, 16 453 plants were scored for egg pre-

sence at the plot level, and for 6187 of these, we also mea-

sured phenotypic traits (Table 1). Lastly, we used the

database from the Swedish Species Gateway to assess how

our sampling periods in S, C, and N regions were related to

local butterfly phenology within each region.

Statistical analyses

At the plot level, we used a generalized linear model

(GLM) with Gaussian error structure and identity link

Table 1 Host plant use in Anthocharis cardamines. The columns show for each species in each region: the number of populations sampled, the

number of A. cardamines eggs found, the number of eggs per sampled plant (total number of eggs on a species in a region/total number of host

plant individuals of this species within the region), the proportion of the total number of eggs laid on each host species, the number of plant

individuals surveyed for eggs and, within brackets, the number in which phenotypic traits were measured. Missing data entries denote plant

species not found in the respective regions

Region Sampled

populations

Host species Number of

Anthocharis eggs

Number of eggs/

plants sampled

Regional proportional

use of host plant (%)

Number of plants

sampled

South Sweden 7 A. thaliana 10 0.009 9.1 1057 (445)

– T. caerulescens – – – –

6 C. bursa-pastoris 6 0.007 5.4 795 (394)

6 C. pratensis 30 0.012 27.3 2307 (587)

4 C. paludosa 11 0.085 10.0 369 (63)

11 A. hirsuta 53 0.032 48.2 1651 (645)

– A. glabra – – – –

Central Sweden 9 A. thaliana 3 0.004 1.5 815 (448)

3 T. caerulescens 7 0.024 3.6 297 (177)

8 C. bursa-pastoris 24 0.043 12.4 556 (331)

3 C. pratensis 21 0.313 10.8 67 (67)

9 C. paludosa 104 0.060 53.6 1746 (682)

7 A. hirsuta 13 0.048 6.7 271 (264)

2 A. glabra 22 0.057 11.3 386 (386)

North Sweden 4 A. thaliana 3 0.004 1.2 827 (415)

7 T. caerulescens 13 0.004 5.3 3132 (365)

3 C. bursa-pastoris 42 0.058 17.3 719 (156)

1 C. pratensis 2 0.011 0.8 180 (177)

4 C. paludosa 130 0.108 53.5 1208 (515)

– A. hirsuta – – – –

1 A. glabra 53 0.757 21.8 70 (70)

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function to study the effects of region and host species

identity on the mean number of eggs per plant. Intra-spe-

cific host plant density was included in the model as a

covariate. The mean number of eggs per plant was log-

transformed, and its variation among regions and host

species was examined with analysis of deviance. We also

examined models including the summed density of all

other potential host plant species in the plots. However,

inter-specific host plant density had no significant

(P = 0.25) effect on the mean number of eggs in a given

species and was not included in the presented models.

At the individual level, we used GLMs with binomial

error structure and logit link function to study the effects of

host region, size, and phenology on egg presence (0 or 1).

The two predictor variables, size and phenology, were the

principal components PC1 and PC2, respectively, extracted

from a principal component analysis (PCA) of the traits

plant size, inflorescence size, and phenological state. We

used PC1 and PC2 instead of the traits because original

trait values were correlated (Pearson, r[0.25, P B 0.05).

PC1 and PC2 explained 48.4 and 32.7% of the variance,

respectively (accumulated explained variance = 81.1%).

PC1 was positively correlated with the plant size and total

number of flowers, whereas PC2 was correlated with the

phenological state. PCA loadings for the three host plant

traits are shown in Table S1 (Electronic Supplementary

Material). As preliminary analyses detected significant

interactions between region and traits for some species, we

evaluated effects of trait variables in separate models for

each region.

Mean ± SE in figures and tables is based on untrans-

formed data. All GLMs were performed with R version 2.6.2

(R Core Team 2008). Multiple comparisons of means (Tukey

contrasts) for the GLMs were made using the multcomp

package (Hothorn et al. 2008). The PCA was carried out with

SPSS 17.0 (SPSS Inc, Chicago, IL, U.S.A.).

RESULTS

Correlations between life history traits and temporal

and latitudinal trends

The average advancement of mean flight date of all 66 but-

terfly species was 0.36 days/year during the last two decades.

Moreover, the mean flight date of the same investigated

butterfly species showed a positive correlation with latitude

(mean value is 1.20 days/degree of latitude). The advance-

ment in mean flight date as well as the seasonal advancement

at lower latitudes was both greater in A. cardamines than in

the vast majority of other butterfly species in the region. It

has advanced its mean flight dates during the last two decades

with a mean value of 1.02 days/year, which is among the top

three of all investigated butterfly species (Fig. 2). In addition,

there are only 2 out of 66 species that show a steeper rela-

tionship between mean flight date and latitude than A.

cardamines (3.41 days/degree of latitude).

Correlations between temporal and spatial trends were also

evident in terms of a significant correlation between the

yearly change in flight date and the dependence of flight date

Fig. 2 The relationship between mean flight date and yearly change in flight date in a set of butterfly species in Sweden during 1991–2010,

r = 0.49, P\0.001 (cf. Table 1 in Karlsson 2013), symbols represent overwintering stage; squares adult, diamonds pupal, crosses larval, and

dots egg. The focal butterfly species, Anthocharis cardamines, in this study is marked with an arrow. The different overwintering stages differ

significantly in respect to degree of yearly change in flight date, F(3,62) = 5.779, P = 0.0015. Redrawn from Karlsson (2013)

S82 AMBIO 2015, 44(Suppl. 1):S78–S88

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on latitude in the 66 species of butterflies investigated (r =

-0.36, P = 0.015; cf. Fig. 5 in Karlsson 2013). In univoltine

species overwintering as pupae, like A. cardamines, this

relationship still holds true (Fig. 3). This suggests that spatial

and temporal variations are partly caused by the same factors

and that investigations of latitudinal trends should be useful to

predict expected future temporal trends in butterfly species.

Since A. cardamines is a univoltine species throughout

its geographic range, it is of interest to restrict the com-

parison to species sharing this characteristic. Among the 66

species investigated by Karlsson (2013), univoltine species

generally have significantly later flight dates compared to

bivoltine species (Fig. 4) (and also compared to adult

overwintering species where adults appear two times per

season but with generally only one cohort of larvae

developing each year) (Fig. 3). Anthocharis cardamines

has a relatively early flight also when compared only to

other univoltine butterfly species; only 2 out of 46 inves-

tigated Swedish univoltine species fly at earlier dates than

A. cardamines. To summarize, our focal species appears

early in the season and much earlier at southern than at

northern latitudes, and has advanced its flight dates in

response to climate warming more strongly than most other

butterfly species in the same area.

Latitudinal variation in use of host plant species

A comparison with the records of A. cardamines during 2010

registered in the Swedish Species Gateway indicated that our

census periods occurred 4–6 days after the peak flight period in

all three regions (Fig. 1). Together with the results of previous

studies showing that the egg stage in the field lasts 7–10 days

(Wiklund and Ahrberg 1978) and that ca. 80% of the eggs are

laid during the first half of the flight season (Wiklund and

Friberg 2009), this strongly suggests that our census provided

accurate assessments of host use in all regions.

The mean number of eggs per plant (number of eggs/

number of plants in each plot) varied among host species

(Table 2; Fig. 5). However, host use differed among the

three regions (significant interaction region 9 species in

Table 2). In the south region, the most used species for

oviposition was C. paludosa, in the central region it was

C. pratensis, and in the north region, A. glabra was the

most attacked species (Fig. 5). From the butterfly’s per-

spective, there was a difference between regions concerning

which host plant was most used for oviposition (Table 1).

Plant phenology and selection of host plants

within species

Among-individual differences in plant resistance to ovi-

position were related to phenology and size, but relation-

ships differed among species and among regions (Fig. 6;

-2 -1 0 1 2 3 4 5 6 7

Latitudinal change in flight date (days/degree of latitude)

-1.1

-1.0

-0.9

-0.8

-0.7

-0.6

-0.5

-0.4

-0.3

-0.2Y

early

cha

nge

in fl

ight

dat

e (d

ays/

year

)

Fig. 3 The relationship between yearly change in mean flight date

and latitudinal change in mean flight date for all 7 species of

butterflies in the dataset that overwinter as pupae and have an

univoltine life cycle, r = -0.77, P = 0.04. Anthocharis cardamines

is second from the right

U B A

Voltinism

22-Apr

2-May

12-May

22-May

1-Jun

11-Jun

21-Jun

1-Jul

11-Jul

21-Jul

Mea

n fli

ght d

ate

1991

-201

0

Fig. 4 Comparison of mean flight date among univoltine (U,

n = 46), bivoltine (B, n = 13), and adult overwintering (A, n = 7)

butterfly species. Mean and SD, F(2,63) = 30.9, P\0.001. Mean

flight date is from Karlsson (2013), and overwintering stage is from

Eliasson et al. (2005)

Table 2 Effects of region, host species identity, and population

density on the mean number of eggs per plant individual in each plot.

Analysis of deviance with region and host species as factors and host

plant density as a covariate

Source of variation Number of eggs per plant

df F P

Region 2 1.816 0.274

Species 6 5.8058 0.001

Density 1 6.88 0.081

Region 9 species 9 3.983 <0.001

Effects significant at P\0.05 are in bold

AMBIO 2015, 44(Suppl. 1):S78–S88 S83

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Table S2 in Electronic Supplementary Material). Plants in

more advance phenological stages were significantly more

attacked in A. thaliana, T. caerulescens, C. pratensis,

A. hirsuta, and A. glabra, while the opposite was true in C.

paludosa. However, the effects of phenology significantly

differed among regions for several species (significant

effects of region 9 phenology in two species and of

region 9 size 9 phenology in two additional species, Table

S2). In T. caerulescens, late-flowering individuals were

more attacked in the north, but there was no significant

effect of phenology in the central region. In C. pratensis,

late-flowering individuals were more attacked in the south

region but there was no effect of phenology in the other

regions. On average, butterflies preferred larger plants in

all host species except for T. caerulescens (Fig. S2).

However, in five of seven species, the effects of size dif-

fered along the latitudinal gradient (significant effects of

region 9 size or region 9 size 9 phenology in Table S2).

There were also significant effects of the interaction

size 9 phenology in four of seven species.

DISCUSSION

There has been a general trend toward earlier flight periods

in Swedish butterflies the last 20 years, and Anthocharis

cardamines is among the species that has advanced its

adult emergence most. Moreover, most Swedish butterfly

species follow the typical pattern of later flight dates in

more northern populations but this cline is steeper in A.

cardamines. This type of correspondence appears to be a

general trend as the rate of phenological change over time

shows a significant correlation with the degree of change in

flight date with latitude. This was true for both the full

dataset with all Swedish butterflies as well as for the sub-

group of univoltine, pupal diapausers, to which A. card-

amines belongs. The results also show the quite intuitive

pattern that butterfly species that are bivoltine start repro-

duction earlier in the year compared to univoltine species.

This is most likely because selection in bivoltine species

favors individuals that can use a longer period of the

favorable season to produce two rather than one generation.

In this respect, the early spring flight period of A. card-

amines is clearly atypical for an univoltine butterfly in

Sweden, occurring on average more than a month earlier

than the other species (May 31 as compared to July 5). The

early emergence of A. cardamines is very probably a direct

consequence of that newly hatch larvae feeds on flowers

and developing fruits of early flowering Brassicaceae

plants.

During the last decades, there have been substantial

phenological changes in a large number of animal and plant

species (Walther et al. 2002; Menzel et al. 2006; Parmesan

2007). As the typical direction of change has been an

advancement of phenological events, it has been causally

linked to recent climate change and in particular the global

Mea

n nu

mbe

r of e

ggs

per p

lant

0.0

0.2

0.4

0.6

0.8

b

a a aa

South locationM

ean

num

ber o

g eg

gs p

er p

lant

0.0

0.2

0.4

0.6

0.8North location *

*

ab

ab

a

a

arth thca cabu capr4 capr8 arhi argl

arth thca cabu capr4 capr8 arhi argl

arth thca cabu capr4 capr8 arhi argl

Mea

n nu

mbe

r of e

ggs

per p

lant

0.0

0.2

0.4

0.6

0.8Central location

c

bcabcab

ababa

NA

NA

b

a a aa

South location

North location *

*

ab

ab

a

a

Central location

c

bcabcab

ababa

NA

NA

Fig. 5 Mean number of eggs per plant (±SE) for seven different host

plant species and three different regions along a latitudinal gradient.

Means among species with different letter are significantly different

(Tukey multiple Comparisons, P\0.05). NA indicates that no popula-

tions of a host species were found in a region. The asterisk denotes that

only one population was found. Species abbreviations: arth = Arabi-

dopsis thaliana), thca = Thlaspi caerulescens, cabu = Capsella bursa-

pastoris, capr4 = Cardamine pratensis), capr8 = Cardamine paludosa,

arhi = Arabis hirsuta, and argl = Arabis glabra

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increase in temperatures (Sparks and Yates 1997; Ste-

fanescu et al. 2003). The results presented here add to this

literature. More interestingly, this study and that of Kar-

lsson (2013) found that the rate of phenological change

over time was correlated with the phenological changes

across latitudes. This suggests that species of butterflies

that show strong latitudinal variation in phenology, pre-

sumably due to spatial variation in climate, also tend to

show strong effects of changes in climate over time. This

correspondence is expected if the adaptations that control

butterfly life cycles and phenology include response to

aspects of climate that changes in a similar way over time

and space, and that populations along the latitudinal gra-

dient respond in similar ways to climatic cues. While

temperature is one obvious and important aspect of cli-

mate, other cues, such as the photoperiod, will not show

this type of parallel change in time and space, i.e., the

photoperiod at a given time of year varies with latitude

while it is not influenced by temporal changes in climate at

any given location. For our particular study system, this

pattern suggests that it is reasonable to use the ‘‘space for

time’’ paradigm to get a rough idea of how climate is likely

to affect the phenology of A. cardamines and how this

might influence its host utilization (Hodgson et al. 2011).

Indeed, it seems likely that both temporal and spatial

changes in the phenology of A. cardamines are reflecting

strong effects of thermal conditions on the hatching of

adults in comparison with other butterfly species. In sup-

port of this idea, the flight date of A. cardamines shows a

strong response to ambient spring temperature during pupal

development where an increase of 1�C advances flight date

with 6.4 days. Mean value for other univoltine butterflies

overwintering in the pupal stage is an advancement of

3.3 days/�C (cf. Karlsson 2013).

The regulation of life cycles of temperate insects is typi-

cally due to plasticity in relation to seasonal cues such as

photoperiod and temperature (Tauber et al. 1986; Nylin and

Gotthard 1998). Given the patterns shown here, it seems

likely that the part of the life cycle determining adult emer-

gence of A. cardamines in the spring is highly dependent on

temperature. As this species spends the overwinter period in

the pupal stage, it is the post-diapause pupal development in

spring that will determine when the adults hatch. Hence,

variation in adult emergence is likely to be strongly affected

by the thermal reaction norms of pupal development. The

advancement of spring phenology during the last decades as

well as the latitudinal variation is likely to be largely a

consequence of plasticity in response to variation in tem-

perature (Gienapp et al. 2008; Merila and Hendry 2014).

However, thermal reaction norms have a genetic basis and

may evolve in response to environmental changes. Indeed,

recent experimental studies demonstrate that thermal reac-

tion norms of post-diapause development in A. cardamines

varies among populations from different latitudes suggesting

that a part of the spatial variation in phenology seen here is

due to local adaptation in these thermal reaction norms

(Posledovich et al. 2014; Stahandske et al. 2014). This also

indicates that natural selection due to consistent directional

change in climatic conditions over time will alter adaptations

that are central for the evolution of phenology. From a cli-

mate change perspective, such evidence of local adaptation

in thermal reaction norms suggests that responses to similar

changes in temperatures will differ between regions along

latitudinal gradients.

-10

12

0 1 0 1 0 1 0 1 0 1

0 10 1

-10

12

-10

12

-10

12

-10

12

-10

12

-10

12

-10

12

-10

12

-10

12

-10

12

-4-2

02

-4-2

02

-4-2

02

-1.5

0.0

1.5

-1.5

0.0

1.5

-20

2-2

02

S

C

NP

heno

logy

arth thca cabu capr4 capr8 arhi argl

*

*

***

*

**

***

***

*

Fig. 6 Box-plots showing the mean phenology (second axis from a PCA, see text) for plant individuals of seven different species and from three

different regions that were either oviposited on by the butterfly Anthocharis cardamines (1) or that escaped attack (0). The seven host plant

species were arth = Arabidopsis thaliana), thca = Thlaspi caerulescens, cabu = Capsella bursa-pastoris, capr4 = Cardamine pratensis),

capr8 = Cardamine paludosa, arhi = Arabis hirsuta, and argl = Arabis glabra. The three regions were: south (S), central (C), and north (N).

Significant differences between groups are indicated by asterisks (*P B 0.05, **P B 0.01, ***P B 0.001). Note that scales differ among species

AMBIO 2015, 44(Suppl. 1):S78–S88 S85

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www.kva.se/en 123

In the field survey examining host plant use of

A. cardamines in three regions along a latitudinal gradient,

we documented significant differences among regions in

which of the host species that were used for oviposition.

Given that the butterfly has strong preferences for plants in

a given phenological stage (Arvanitis et al. 2008; this

study), it is likely that effects of climate on the temporal

overlap between the butterfly and each of the host plant

species were important for these among-region differences.

Such differences in temporal overlap between the butterfly

and the different host plant species in response to latitu-

dinal variation in temperature are to be expected if the

thermal reaction norms differ between host plants and

between the butterfly and its preferred host plants. It might

seem reasonable to assume that phenological specialists,

such as A. cardamines, are particularly sensitive to changes

in climate. However, while the butterfly is expected to be

under strong selection to match its phenology with the

temporal distribution of Brassicaceae flowers in the spring,

it is simultaneously strongly selected to be able to use

multiple hosts given that the temporal overlap with one

given species varies among years (Wiklund and Friberg

2009). As a result, the specialized feeding on the young

fruits and seeds of its hosts is combined with the ability to

utilize a quite wide host range of Brassicaceae species.

Such a notion, that the species can be characterized as a

phenological specialist but a host species generalist, is

strongly supported not only by our data on latitudinal

variation in host use but also by data on between-year

variation in host use at a given site. During a 5-year study

of the species at one locality in Sweden (the central loca-

tion in this study), the species oviposited on 16 of the 18

available Brassicaceae species (Wiklund and Friberg

2009). A tentative conclusion is therefore that an assumed

sensitivity of herbivores specializing in particular pheno-

logical stages of their host plants to climatic variation

might sometimes be buffered by an ability to switch host

plant species. If such host plant switching does not occur,

we should expect very strong selection on consumer

reaction norms to match the reaction norms of their

resources.

Our results also show that within species, the pheno-

logical state and size of the hosts at the time of butterfly

reproduction are important for oviposition. For most of the

plant species, we found that later-flowering individuals

attracted more eggs, although in one of the main hosts,

C. paludosa, early flowering plants were significantly more

used for oviposition. These results are important in two

respects. First, they provide further evidence that pheno-

logical stage is important for butterfly host plant selection

and that not only among-species choice but also choices

within species are influenced by the phenological stage of

the host plant. Moreover, several within-species patterns

varied among regions suggesting that the exact temporal

overlap between butterfly oviposition and host plant flow-

ering had a strong effect on the realized host use across the

climatic gradient described by the latitudinal range and that

this overlap differed among regions. This suggests that the

effect of climatic variation on host plant phenology, both in

space and over time, will be of major importance for the

realized host use of A. cardamines. Second, given that

butterfly attack has strong negative effects on plant fitness

(Konig 2014), the documented patterns of butterfly pref-

erences translate to butterfly-mediated selection on plant

flowering phenology. Given that butterfly attacks are rel-

atively frequent in host plant populations, our documented

patterns suggest that butterfly-mediated selection on plant

flowering phenology may differ not only among different

host plant species but also among regions within species.

CONCLUSION

Anthocharis cardamines shows a strong phenological

response to climatic variation compared to most other but-

terfly species that share its life history characteristics (uni-

voltinism, pupal diapause). This pattern, in combination

with it being a phenological specialist but a host species

generalist, leads to substantial variation in host use both in

time (Wiklund and Friberg 2009) and in space (this study).

Unless the guild of its host plant species shows a very

similar phenological alteration with the ongoing change in

climate, which has been suggested for at least Alliaria pet-

iolata and Cardamine pratensis in the UK (Sparks and Yates

1997), the realized host use of the butterfly is likely to be

affected. However, the pattern of spatial variation in host use

demonstrated here indicates that the species as a whole

appears to harbor the necessary genetic variation, allowing it

to respond both ecologically and evolutionarily to a rela-

tively large range of climatic variation.

Acknowledgment This study was funded by the Strategic Research

Programme Ekoklim at Stockholm University.

Open Access This article is distributed under the terms of the

Creative Commons Attribution License which permits any use, dis-

tribution, and reproduction in any medium, provided the original

author(s) and the source are credited.

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AUTHOR BIOGRAPHIES

Jose A. Navarro-Cano was granted by the Seneca Foundation (fel-

lowship 12337/PD/09) for participating in the Ekoklim Program. He

is currently a postdoc researcher at the Desertification Research

Centre (CIDE, CSIC-UVEG-GV) from Valencia (Spain). His research

interests include functional and applied ecology of the inter-specific

interactions and global change ecology.

Address: Department of Ecology, Environment and Plant Sciences,

Stockholm University, 106 91 Stockholm, Sweden.

e-mail: [email protected]

Bengt Karlsson is a full Professor at the Department of Zoology,

Stockholm University. His research interests include climate change

and phenology, evolutionary ecology, and butterfly life history

strategies.

Address: Department of Zoology, Stockholm University, 106 91

Stockholm, Sweden.

e-mail: [email protected]

Diana Posledovich is a PhD student in ecology at the Department of

Zoology at Stockholm University. Her research focuses on spatial

aspects of host plant utilization in butterflies and on mechanism for

phenological synchronization of butterfly and their host plants.

Address: Department of Zoology, Stockholm University, 106 91

Stockholm, Sweden.

e-mail: [email protected]

Tenna Toftegaard is a PhD student at Stockholm University,

Department of Ecology, Environment and Plant Sciences. Her

research interests include plant–insect interactions and climate

change.

Address: Department of Ecology, Environment and Plant Sciences,

Stockholm University, 106 91 Stockholm, Sweden.

e-mail: [email protected]

Christer Wiklund is professor emeritus at the Department of Zool-

ogy, Stockholm University. He is an evolutionary ecologist whose

research is focused on the behavioral ecology of butterflies, with

particular reference to host plant use, life history strategies, and

defense against predation.

Address: Department of Zoology, Stockholm University, 106 91

Stockholm, Sweden.

e-mail: [email protected]

Johan Ehrlen is a Professor at the Department of Ecology, Envi-

ronment and Plant Sciences at Stockholm University. His research

interests include plant–animal interactions, plant life history evolu-

tion, and plant population dynamics.

Address: Department of Ecology, Environment and Plant Sciences,

Stockholm University, 106 91 Stockholm, Sweden.

e-mail: [email protected]

Karl Gotthard (&) is a researcher and Associate Professor at the

Department of Zoology at Stockholm University. His research inter-

ests include evolution and ecology of seasonal adaptations in insects,

with particular reference to adaptive plasticity and local adaptation in

life history traits.

Address: Department of Zoology, Stockholm University, 106 91

Stockholm, Sweden.

e-mail: [email protected]

S88 AMBIO 2015, 44(Suppl. 1):S78–S88

123� The Author(s) 2015. This article is published with open access at Springerlink.com

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